Abstract
Eelgrass Zostera marina is an ecosystem-engineering species of outstanding importance for coastal soft sediment habitats that lives in widely diverging habitats. Our first goal was to detect divergent selection and habitat adaptation at the molecular genetic level; hence, we compared three pairs of permanently submerged versus intertidal populations using genome scans, a genetic marker-based approach. Three different statistical approaches for outlier identification revealed divergent selection at 6 loci among 46 markers (6 SNPs, 29 EST microsatellites and 11 anonymous microsatellites). These outlier loci were repeatedly detected in parallel habitat comparisons, suggesting the influence of habitat-specific selection. A second goal was to test the consistency of the general genome scan approach by doubling the number of gene-linked microsatellites and adding single nucleotide polymorphism (SNP) loci, a novel marker type for seagrasses, compared to a previous study. Reassuringly, results with respect to selection were consistent among most marker loci. Functionally interesting marker loci were linked to genes involved in osmoregulation and water balance, suggesting different osmotic stress, and reproductive processes (seed maturation), pointing to different life history strategies. The identified outlier loci are valuable candidates for further investigation into the genetic basis of natural selection.
Similar content being viewed by others
References
Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA et al (2004) Population history and natural selection shape patterns of genetic variation in 132 genes. PLOS Biol 2:1591–1599
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29
Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980
Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc Biol Sci 263:1619–1626
Bonin A, Taberlet P, Miaud C, Pompanon F (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol Biol Evol 23:773–783
Bouck A, Vision T (2007) The molecular ecologist’s guide to expressed sequence tags. Mol Ecol 16:907–924
Campbell D, Bernatchez L (2004) Genomic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21:945–956
Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B et al (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260
den Hartog C (1970) The seagrasses of the world. Verh K Ned Akad We. Afd Natuurkd II 59:1–275
Dieringer D, Schlötterer C (2003) MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169
Duarte CM (2002) The future of seagrass meadows. Environ Cons 29:192–206
Egan SP, Nosil Patrik, Funk DanielJ (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62:1162–1181
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Ferber S, Reusch TBH, Stam WT, Olsen JL (2008) Characterization of single nucleotide polymorphism markers for eelgrass (Zostera marina). Mol Ecol Resour 8:1429–1435
Glaubitz JC, Rhodes OE, Dewoody JA (2003) Prospects for inferring pairwise relationships with single nucleotide polymorphisms. Mol Ecol 12:1039–1047
Harr B, Kauer M, Schlötterer C (2003) Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophila melanogaster (vol 99, pg 12949, 2002). Proc Natl Acad Sci USA 100:3004
Harris MA, Clark JI, Ireland A, Lomax J, Ashburner M, Collins R et al (2006) The gene ontology (GO) project in 2006. Nucleic Acids Res 34:D322–D326
Hemminga M, Duarte C (2000) Seagrass ecology. Cambridge University Press, Cambridge
Kane NC, Rieseberg LH (2007) Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics 175:1823–1834
Kauer MO, Dieringer D, Schlötterer C (2003) A microsatellite variability screen for positive selection associated with the “Out of Africa” habitat expansion of Drosophila melanogaster. Genetics 165:1137–1148
Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of theory of selective neutrality of polymorphisms. Genetics 74:175–195
Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994
Luu D-T, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96
Mäkinen HS, Cano JM, Merilä J (2008) Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback Gasterosteus aculeatus populations. Mol Ecol 17:3565–3582
Massa SI, Arnaud-Haond S, Pearson GA, Serrao E (2009) Temperature tolerance and survival of intertidal populations of the seagrass Zostera noltii (Hornemann) in southern Europe (Ria Formosa, Portugal). Hydrobiologia. doi:http://doi.org/10.1007/s10750-008-9609-4
Namroud M-C, Beaulieu Jean, Juge Nicolas, Laroche Jerome, Bousquet Jean (2008) Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Mol Ecol 17:3599–3613
Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218
Oetjen K, Reusch TBH (2007) Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol Ecol 16:5156–5157
Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Bostrom C et al (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol Ecol 13:1923–1941
Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996
Ouborg NJ, Vriezen WH (2007) An ecologist’s guide to ecogenomics. J Ecol 95:8–16
Reise K (1985) Tidal flat ecology: an experimental approach to species interactions. Springer, Berlin
Reise K, Jager Z, De Jong D, Van Katwijk M, Schanz A (2005) Seagrass—Wadden Sea ecosystem no. 19. Common Wadden Sea Secretariat, Wilhelmshaven
Rengmark AH, Slettan A, Skaala O, Lie O, Lingaas F (2006) Genetic variability in wild and farmed Atlantic salmon (Salmo salar) strains estimated by SNP and microsatellites. Aquaculture 253:229–237
Reusch TBH (2002) Microsatellites reveal high population connectivity in eelgrass (Zostera marina) in two contrasting coastal areas. Limnol Oceanogr 47:78–85
Reusch TBH, Veron AS, Preuss C, Weiner J, Wissler L, Beck A et al (2008) Comparative analysis of expressed sequence tag (EST) libraries in the seagrass Zostera marina subjected to temperature stress. Mar Biotechnol 10:297–309
Ryynanen HJ, Tonteri A, Vasemagi A, Primmer CR (2007) A comparison of Biallelic markers and microsatellites for the estimation of population and conservation genetic parameters in Atlantic Salmon (Salmo salar). J Hered 98:692–704
Schlötterer C (2002a) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160:753–763
Schlötterer C (2002b) Towards a molecular characterization of adaptation in local populations. Curr Opin Genet Dev 12:683–687
Schlötterer C (2003) Hitchhiking mapping—functional genomics from the population genetics perspective. Trends Genet 19:32–38
Scotti-Saintagne C, Mariette S, Porth I, Goicoechea PG, Barreneche T, Bodenes K et al (2004) Genome scanning for interspecific differentiation between two closely related oak species Quercus robur L. and Q. petraea (Matt.) Liebl. Genetics 168:1615–1626
Silander JA (1979) Microevolution and clone structure in Spartina patens. Science 203:658–660
Smith JM, Haigh J (1974) Hitch-hiking effect of a favorable gene. Genet Res 23:23–35
Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170
Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688
Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genome Res 16:702–712
Thornton KR, Jensen JD (2007) Controlling the false-positive rate in multilocus genome scans for selection. Genetics 175:737–750
Tsumura Y, Kado T, Takahashi T, Tani N, Ujino-Ihara T, Iwata H (2007) Genome scan to detect genetic structure and adaptive genes of natural populations of Cryptomeria japonica. Genetics 176:2393–2403
van Katwijk MM, Hermus DCR (2000) Effects of water dynamics on Zostera marina: transplantation experiments in the intertidal Dutch Wadden Sea. Mar Ecol Prog Ser 208:107–118
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vasemagi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol Biol Evol 22:1067–1076
Vitalis R, Dawson K, Boursot P (2001) Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811–1823
Vitalis R, Dawson K, Boursot P, Belkhir K (2003) DetSel 1.0: a computer program to detect markers responding to selection. J Hered 94:429–431
Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619
Wissler L, Dattolo E, Moore AD, Reusch TBH, Olsen JL, Migliaccio M, Bornberg-Bauer E, Procaccini G (2009) Dr. Zompo: an online data repository for Zostera marina and Posidonia oceanica ESTs. Database 2009: bap009
Acknowledgments
We thank B. Hasert for technical assistance. Many thanks to Prof. Karsten Reise from AWI Sylt for help and support, as well as to Andreas Zipperle for help collecting samples. This work was funded by Max-Planck society and the DFG (grant no. Re 1108/7-1).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Uthicke.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Oetjen, K., Ferber, S., Dankert, I. et al. New evidence for habitat-specific selection in Wadden Sea Zostera marina populations revealed by genome scanning using SNP and microsatellite markers. Mar Biol 157, 81–89 (2010). https://doi.org/10.1007/s00227-009-1297-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-009-1297-8